The accessory organ,a scolopidial sensory organ,in the cave cricket Troglophilus neglectus (Orthoptera: Ensifera: Rhaphidophoridae)

Mechanoreceptor organs occur in great diversity in insect legs. This study investigates sensory organs in the leg of atympanate cave crickets (Troglophilus neglectus KRAUSS, 1879) by neuronal tracing. Previously, the subgenual and the intermediate organs were recognised in the subgenual organ complex, lacking the tympanal membranes present for example in the tibial hearing organs of Gryllidae and Tettigoniidae. We document the presence of the accessory organ in T. neglectus. This scolopidial organ is located in the posterior tibia close to the subgenual organ and can be identified by position, innervation and orientation of the dendrites of sensory neurons. The main motor nerve in the leg innervates a part of the subgenual organ and the accessory organ. The dendrites of sensory neurons in the accessory organ are characteristically bent in proximo‐dorsal direction, while the subgenual organ dendrites run distally along the longitudinal axis of the leg. The accessory organ contains 6–10 scolopidial sensilla, and no differences in neuroanatomy occur between the three thoracic leg pairs. Hence, the subgenual organ complex in cave crickets is more complex than previously known. The wider taxonomic distribution of the accessory scolopidial organ among orthopteroid insects is inconsistent, indicating its repeated losses or convergent evolution.     

The scolopidial accessory organ in the Jerusalem cricket (Orthoptera: Stenopelmatidae)

Multiple mechanosensory organs form the subgenual organ complex in orthopteroid insects, located in the proximal tibia. In several Ensifera (Orthoptera), a small chordotonal organ, the so-called accessory organ, is the most posterior part of this sensory complex. In order to document the presence of this accessory organ among the Ensifera, the chordotonal sensilla and their innervation in the posterior tibia of two species of Jerusalem crickets (Stenopelmatidae: Stenopelmatus) is described. The sensory structures were stained by axonal tracing. Scolopidial sensilla occur in the posterior subgenual organ and the accessory organ in all leg pairs. The accessory organ contains 10–17 scolopidial sensilla. Both groups of sensilla are commonly spatially separated. However, in few cases neuronal fibres occurred between both organs. The two sensillum groups are considered as separate organs by the general spatial separation and innervation by different nerve branches. A functional role for mechanoreception is considered: since the accessory organ is located closely under the cuticle, sensilla may be suited to detect vibrations transferred over the leg's surface. This study extends the known taxa with an accessory organ, which occurs in several taxa of Ensifera. Comparative neuroanatomy thus suggests that the accessory organ may be conserved at least in Tettigoniidea.     

Central projections of sensory cells of the midleg of the locust,Schistocerca gregaria

The central projections of trichoid hairs and of some scolopidial organs of the mesothoracic leg of the locust Schistocerca gregaria were studied by using nickel chloride backfilling and single cell recording. Trichoid hair sensilla on different parts of the legs project somatotopically in the ventral part of the ipsilateral neuropile of the mesothoracic ganglion. Generally, distally located receptors have their terminal arborizations in ventro-lateral areas of the neuropile, and proximally located receptors in ventro-medial areas. The axons of the subgenual organ and tarsal chordotonal organs project into the intermediate neuropile.     

The scolopidial accessory organs and Nebenorgans in orthopteroid insects: Comparative neuroanatomy,mechanosensory function,and evolutionary origin

Scolopidial sensilla in insects often form large sensory organs involved in proprioception or exteroception. Here the knowledge on Nebenorgans and accessory organs, two organs consisting of scolopidial sensory cells, is summarised. These organs are present in some insects which are model organisms for the physiology of mechanosensory systems (cockroaches and tettigoniids). Recent comparative studies documented the accessory organ in several taxa of Orthoptera (including tettigoniids, cave crickets, Jerusalem crickets) and the Nebenorgan in related insects (Mantophasmatodea). The accessory organ or Nebenorgan is usually a small organ of 8–15 sensilla located in the posterior leg tibia of all leg pairs. The physiological properties of the accessory organs and Nebenorgans are so far largely unknown. Taking together neuroanatomical and electrophysiological data from disparate taxa, there is considerable evidence that the accessory organ and Nebenorgan are vibrosensitive. They thus complement the larger vibrosensitive subgenual organ in the tibia. This review summarises the comparative studies of these sensory organs, in particular the arguments and criteria for the homology of the accessory organ and Nebenorgan among orthopteroid insects. Different scenarios of repeated evolutionary origins or losses of these sensory organs are discussed. Neuroanatomy allows to distinguish individual sensory organs for analysis of sensory physiology, and to infer scenarios of sensory evolution.     

The structure and properties of an abdominal chordotonal organ in Carausius morosus and Blaberus discoidalis

Each side of the abdominal segments of the stick insect Carausius morosus contains a chordotonal organ lying longitudinally in a ventro-lateral position. These ventro-lateral chordotonal organs each possess two nerve cell bodies and two scolopales. There is a single attachment strand to the cuticle.Electrical recordings from the receptors show that they respond in a highly phasic manner to both stretching and subsequent relaxation of the attachment strand. They are sensitive to substrate vibration but are activated by ventilatory movements. The effects of ramp and square wave stimulation are examined. The rôle of the ventro-lateral chordotonal organs as ventilatory receptors is discussed and abdominal chordotonal organs of insects in general are reviewed.The ‘ventral phasic receptors’ of the cockroach are re-examined and shown to be chordotonal organs. They are re-named ‘mid-ventral’ chordotonal organs.     

The fine structure of the cockroach subgenual organ

This paper describes the fine structure of the cockroach subgenual organ, a complex ciliated mechanoreceptor that detects vibrations in the substrate upon which the animal stands. Located beneath the knee in each walking leg, the cockroach subgenual organ is a thin, fan-shaped flap of tissue slung across the dorsal blood space of the tibia at right angles to the leg's long axis. It is innervated by approximately 50 chordotonal sensilla. The fine structure of the chordotonal sensilla is is described in detail ; possible transducer sites are discussed.     

Range fractionation in the locust metathoracic femoral chordotonal organ

Summary Insect femoral chordotonal organs are internal proprioceptors which monitor the position and movements of the femur-tibia joint of the leg. The locust (Locusta migratoria) metathoracic femoral chordotonal organ is composed of approximately 100 neurones with a variety of response properties. In this study intracellular recordings were used to examine the range fractionation of phasic and tonic responses to tibial movements. Some neurones responded across the full range of leg angles, while others had restricted response ranges, and could therefore act as labeled lines. Neurones with maximal firing at mid-angles are described for the first time in a locust femoral chordotonal organ. Responses are discussed in terms of underlying structural constraints on signal transduction.Abbreviation (mt) FCO (metathoracic) femoral chordotonal organ     

Responses and locations of neurones in the locust metathoracic femoral chordotonal organ

Summary Insect legs possess chordotonal organs which monitor leg angle, and the direction, velocity and acceleration of leg movements. The locust metathoracic femoral chordotonal organ (mtFCO) has previously been studied morphologically and physiologically, but no detailed analysis of the responses of individual neurones, and their location in the organ has so far been produced. By recording from, and staining mtFCO neurones I have been able to compile for the first time such a map. The distribution of neurone somata in the locust mtFCO is more complex than previously thought: receptors sensitive to both stretch and relaxation of the apodeme are distributed throughout the organ. Seventeen response types were encountered. Neurones with a particular response type have somata in comparable locations within the mtFCO. Comparisons are made between the response types found in the stick insect and those in the locust. The possible functions of some of the responses are discussed.Abbreviation (mt)FCO (metathoracic) femoral chordotonal organ - F-T femur-tibia     

The contributions of diverse sense organs to the control of leg movement by a walking insect

Summary During locomotion, stick insectsCarausius morosus, place the tarsus of the rear leg near the tarsus of the ipsilateral middle leg, whatever the position of the latter. This adjustment by the hind leg requires that it receive information on the actual position of the middle leg tarsus. It is shown by ablation experiments that such information is contributed by the following proprioceptors of the middle leg: the ventral and dorsal coxal hairplates, the coxal hair rows, the trochanteral hairplate and the femoral chordotonal organ. Additional information comes from other, as yet unidentified, sense organs. Several alternatives are considered to explain how the signals from the diverse sense organs of the subcoxal joint might be combined in computing the target position for the protracting hind leg. The experimental results support the hypothesis that the signals are added nonlinearly and that a signal deviating from the majority pattern is weighted less.Abbreviations cxHPu ventral coxal hairplate - cxHPd dorsal coxal hairplate - trHP trochanteral hairplate - HR hair row - feCO femoral chordotonal organ - AEP anterior extreme position     

Neurophysiology of the vibration sense in locusts and bushcrickets: Response characteristics of single receptor units

The response characteristics of the vibration receptors in the legs of the migratory locust, Locusta migratoria, and the tettigoniid Decticus verrucivorus were investigated electro-physiologically by single cell recordings. The legs were stimulated by sinusoidal vibrations. There are four types of vibration receptor in each leg of Locusta and Decticus, which can be classified physiologically. One type—most probably campaniform sensilla—shows a phase-locked response to vibrations from 30 to 200 Hz, its threshold reflecting the displacement. A second type shows similar responses in the same frequency range, but its reactions depend on the stimulus acceleration. The receptor cells of the subgenual organ are very sensitive to vibration from 30 to at least 5000 Hz, and their responses depend on acceleration. There are two types of subgenual receptors, one of which shows a clear maximum of sensitivity between 200 and 1000 Hz, with a threshold below 0.01 m/sec^?2 acceleration. Subgenual receptors with different thresholds and different characteristic frequencies occur in each leg. The receptors of each leg pair have quite similar mean sensitivities and characteristic frequencies. However, in the front legs of tettigoniids the more sensitive subgenual receptors and an additional receptor type also respond to low-frequency airborne sound up to 10 kHz.     

The development of the sensory organs of the legs in the blowfly,Phormia regina

Summary The development of the sensory neurons of the legs of the blowfly,Phormia regina has been described from the third instar larva to the late pupa using immunohistochemical staining. The leg discs of the third instar larva contain 8 neurons of which 5 come to lie in the fifth tarsomere of the developing leg. Whereas 2 neurons persist at least to the late pupa, the other cells degenerate. The first neurons of gustatory sensilla arise in the fifth tarsomere at about 1.5 h after formation of the puparium. Most of these sensilla, however, appear within a short time period beginning at about 18 h. The femoral chordotonal sensory neurons first appear at the time of formation of the puparium, as a mass of cells situated in the distal femur. During later pupal development 2 groups of these cells come to lie at the femur-trochanter border, where they become the proximal femoral chordotonal organ of the adult; the remaining cells become the distal femoral chordotonal organ. Other scolopidial neurons appear later in development. The nerve pathways of the late pupal leg are established either by the axons of the cells that are present in the larval leg disc or by new outgrowing processes of sensory neurons. In the tibia, the initial direction of new outgrowth differs in different regions of the segment: proximal tibial neurons grow distally, while distal tibial neurons grow initially proximally.     

Fine structure of the tibiotarsal and pretarsal sensory organs in Monobella grassei banyulensis Deharveng (Collembola : Neanuridae)

The fine structure of the tibiotarsal and pretarsal sensory organs of Monobella grassei banyulensis Deharveng (Collembola : Neanuridae) has been examined by electron microscopy.Three types of sensory organs have been observed. (1) the most numerous setae of the tibiotarsus are classic mechanosensitive setae with one bipolar sensory cell, whose distal outer segment ends in a tubular body. (2) Two small setae are arranged on each side of the basal part of the claw; they show 3 sensory cells, 2 of which are mechanosensitive cells of the scolopidial type; the outer segments of the 2 mechanosensitive cells end at the base of the sensory hair. The dendrite of the 3rd sensory cell extends into the hair shaft. (3) Two similar chordotonal sensilla link the tibiotarsus and the pretarsus; each sensillum is composed of 2 bipolar sensory cells enveloped in sheath cells. The first type of sensory organ shows the characteristics of insect exteroceptive mechanosensitive hairs. The mechanosensitive cells of the 2nd and 3rd tibiotarsus sensory organs are probably proprioceptive and control the movements of the pretarsus in relation to the tibiotarsus. Two features are noteworthy: (1) the association of the scolopidial cells with a chemosensitive one has never been observed in other insect sensory organs, except in the Collembola; and (2) there is an important morphological diversity in the ciliary roots of the various scolopidial cells, which are in other respects very similar.     

Comparison of auditory sense organs in parasitoid Tachinidae (Diptera) hosted by Tettigoniidae (Orthoptera) and homologous structures in a non-hearing Phoridae (Diptera)

The dipteran parasitoids Therobia leonidei and Homotrixa alleni (Tachinidae) use acoustic cues to locate their calling tettigoniid (Ensifera, Orthoptera) hosts. The sexually dimorphic tympanal organs of both fly species are located at the prosternum. For comparison a homologous chordotonal organ in the non-hearing fly Phormia regina, Meigen (Phoridae) is also described. The scolopidial sense organs of the ears have approximately 180 sensory cells in Th. leonidei and 250 cells in H. alleni. Interspecific analysis indicates that the cell number and arrangement might be genus specific in Tachinidae. The mononematic scolopidia, each with one sensory cell, are of different sizes and insert at the tympanal membrane. Large scolopidial units (diameter of sensory cells up to 50 μm) extend longitudinally from the centre of the sensory organ towards the ligament, whereas small units (sensory cell diameter up to 10 μm) are arranged sequentially within the sensory organ. This arrangement is discussed to be a possible basis for frequency discrimination. The ultrastructure of the scolopidia is similar in the hearing and non-hearing flies. In both groups, the majority of scolopales has a diameter from 2 to 2.9 μm, although hearing species have additionally wider scolopales. The homologous chordotonal organ of Ph. regina consists of approximately 55 sensory cells of uniform direction. The data are discussed in comparison to the ears of other Diptera.     

Biophysics of the subgenual organ of the honeybee, Apis mellifera

The subgenual organ of the honeybee (Apis mellifera) is suspended in a haemolymph channel in the tibia of each leg. When the leg is accelerated, inertia causes the haemolymph (and the subgenual organ) to lag behind the movement of the rest of the leg. The magnitude of this phase lag determines the displacement of the subgenual organ relative to the leg and to the proximal end of the organ, which is connected to the cuticle. Oscillations of the subgenual organ are visualised during vibration stimulation of the leg, by means of stroboscopic light. Video analysis provides fairly accurate values of the amplitude and phase of the oscillations, which are compared with the predictions of a model.   The model comparison shows that the haemolymph channel can be described as an oscillating fluid-filled tube occluded by an elastic structure (probably the subgenual organ). The mechanical properties of the subgenual organ and haemolymph channel resemble those of an overdamped mass-spring system. A comparison of the threshold curve of the subgenual organ determined using electrophysiology with that predicted by the oscillating tube model suggests that the sensory cells respond to displacements of the organ relative to the leg. Accepted: 10 May 1997     

Development of leg chordotonal sensory organs in normal and heat shocked embryos of the cricket Teleogryllus commodus (Walker)

This paper describes the embryonic development of some parts of the sensory peripheral nervous system in the leg anlagen of the cricket Teleogryllus commodus in normal and heat shocked embryos. The first peripheral neurons appear at the 30% stage of embryogenesis. These tibial pioneer neurons grow on a stereotyped path to the central nervous system and form a nerve which is joined by the growth cones of axons that arise later, including those from the femoral chordotonal organ, subgenual organ and tympanal organ. The development of these organs is described with respect to the increase in number of sensory receptor cells and the shape and position of the organs. At the 100% stage of embryogenesis all three organs have completed their development in terms of the number of sense cells and have achieved an adult shape. To study the function of the tibial pioneer neurons during embryogenesis a heat shock was used to prevent their development. Absence of these neurons has no effect on the development of other neurons and organs proximal to them. However, the development of distal neurons and organs guided by them is impaired. The tibial pioneer neurons grow across the segmental boundary between femur and tibia early in development, and the path they form seems to be essential for establishing the correct connections of the distal sense organs with the central nervous system.     

Physiology of vibration-sensitive afferents in the femoral chordotonal organ of the stick insect

The femoral chordotonal organ in orthopterans signals proprioceptive sensory information concerning the femur-tibia joint to the central nervous system. In the stick insect, 80 out of 500 afferents sense tibial position, velocity, or acceleration. It has been assumed that the other sensory cells in the chordotonal organ would serve as vibration detectors. Extracellular recordings from the femoral chordotonal organ nerve in fact revealed a sensitivity of the sense organ for vibrations with frequencies ranging from 10 Hz to 4 kHz, with a maximum sensitivity between 200 and 800 Hz. Single vibration-sensitive afferents responded to the same range of frequencies. Their spike activity depended on acceleration amplitude and displacement amplitude of the vibration stimulus. Additionally, 80% of the vibration-sensitive afferents received indirect presynaptic inputs from themselves or from other afferents of the femoral chordotonal organ, the amplitude of which depended on stimulus frequency and displacement amplitude. They were associated with a decrease of input resistance in the afferent terminal. From the present investigation we conclude that the femoral chordotonal organ of the stick insect is a bifunctional sensory organ that, on the one hand, measures position and movement of the tibia and, on the other hand, detects vibration of the tibia. Accepted: 6 November 1998     

Evolution of the metathoracic tympanal ear and its mesothoracic homologue in the Macrolepidoptera (Insecta)

Two independent methods of comparison, serial homology and phylogenetic character mapping, are employed to investigate the evolutionary origin of the noctuoid moth (Noctuoidea) ear sensory organ. First, neurobiotin and Janus green B staining techniques are used to describe a novel mesothoracic chordotonal organ in the hawkmoth, Manduca sexta, which is shown to be serially homologous to the noctuoid metathoracic tympanal organ. This chordotonal organ comprises a proximal scolopidial region with three bipolar sensory cells, and a long flexible strand (composed of attachment cells) that connects peripherally to an unspecialized membrane ventral to the axillary cord of the fore-wing. Homology to the tympanal chordotonal organ in the Noctuoidea is proposed from anatomical comparisons of the meso- and metathoracic nerve branches and their corresponding peripheral attachment sites. Second, the general structure (noting sensory cell numbers, gross anatomy, and location of peripheral attachment sites) of both meso- and metathoracic organs is surveyed in 23 species representing seven superfamilies of the Lepidoptera. The structure of the wing-hinge chordotonal organ in both thoracic segments was found to be remarkably conserved in all superfamilies of the Macrolepidoptera examined except the Noctuoidea, where fewer than three cells occur in the metathoracic ear (one cell in representatives of the Notodontidae and two cells in those of other families examined), and at the mesothoracic wing-hinge (two cells) in the Notodontidae only. By mapping cell numbers onto current phylogenies of the Macrolepidoptera, we demonstrate that the three-celled wing-hinge chordotonal organ, believed to be a wing proprioceptor, represents the plesiomorphic state from which the tympanal organ in the Noctuoidea evolved. This ’trend toward simplicity’ in the noctuoid ear contrasts an apparent ’trend toward complexity’ in several other insect hearing organs where atympanate homologues have been studied. The advantages to having fewer rather than more cells in the moth ear, which functions primarily to detect the echolocation calls of bats, is discussed. Accepted: 18 June 1999     

Processing of vibratory and acoustic signals by ventral cord neurones in the cricket Gryllus campestris

The responses of single vibratory receptors and ascending ventral cord interneurones were studied extracellularly in Gryllus campestris L. The physiology of the vibration receptors resembled those found in tettigoniids and locusts. The frequency responses of the subgenual receptors provide two possible cues for central frequency discrimination: differences in mean tuning between groups of receptors in the different leg pairs and a range of receptors tuned to different frequencies within one subgenual organ.Most of the ascending vibratory interneurones were highly sensitive in either the low or high frequency range. Broadbanded neurones were less sensitive. The characteristic sensitivity peaks of these units are due mainly to receptor inputs from a particular leg pair, although most central neurones receive inputs from all 6 legs. Only one neurone type, TN1 received excitatory inputs from both auditory and vibratory receptors; its responses were greatly enhanced by the simultaneous presentation of both stimulus modes. The responses to sound stimuli of AN2, on the other hand, were inhibited by vibration. No other auditory interneurones investigated were influenced by inputs from vibration receptors. Central processing of vibratory information in the cricket is compared with that of tettigoniids and locusts.     

Evolution and Diversity of Vibrational Signals in Mantophasmatodea (Insecta)

Vibrational communication for species identification and mate location is widespread among insects. We investigated the vibrational communication signals of 13 species of the insect order Mantophasmatodea (Heelwalkers). Males and females produce percussive signals by tapping their abdomens on the substrate to locate conspecific mates. We show that male and female calls are of similar general structure but differ in temporal characteristics. Using a principal component analysis, we demonstrate that most species can be distinguished by their calls only. Mapping the calls onto an existing molecular phylogenetic tree reveals a slow diverging drift of male call pattern but no specific trend. For females, a trend from faster towards slower pulse repetition times is indicated. Two sympatric species, Karoophasma biedouwense and Viridiphasma clanwilliamense (Austrophasmatidae), exhibit very different call parameters. The latter species produces calls rather different from all other investigated species, which might hint at reproductive character displacement.     

Interaction between descending input and thoracic reflexes for joint coordination in cockroach: I. Descending influence on thoracic sensory reflexes

Tethered cockroaches turn from unilateral antennal contact using asymmetrical movements of mesothoracic (T2) legs (Mu and Ritzmann in J Comp Physiol A 191:1037–1054, 2005). During the turn, the leg on the inside of the turn (the inside T2 leg) has distinctly different motor patterns from those in straight walking. One possible neural mechanism for the transformation from walking to inside leg turning could be that the descending commands alter a few critical reflexes that start a cascade of physical changes in leg movement or posture, leading to further alterations. This hypothesis has two implications: first, the descending activities must be able to influence thoracic reflexes. Second, one should be able to initiate the turning motor pattern without descending signals by mimicking a point farther down in the reflex cascade. We addressed the first implication in this paper by experiments on chordotonal organ reflexes. The activity of depressor muscle (Ds) and slow extensor tibia muscle (SETi) was excited and inhibited by stretching and relaxing the femoral chordotonal organ. However, the Ds responses were altered after eliminating the descending activity, while the SETi responses remain similar. The inhibition to Ds activity by stretching the coxal chordotonal organ was also altered after eliminating the descending activity.